Syst Biol. This date is consistent with previous inferences about the origin of fig and pollinator mutualism [4]. The genetic template was already present. 2012, 66: 2723-2738. Rentsch, J. D., and J. Leebens-Mack. Ecol Monogr 71:511530, Friberg M, Schwind C, Roark LC, Raguso RA, Thompson JN (2014) Floral scent contributes to interaction specificity in coevolving plants and their insect pollinators. Matsuo T: Genes for host-plant selection in Drosophila. A NanoDrop ND-1000 Spectrophotometer (Nano-Drop Technologies, Wilmington, DE, USA) was used to confirm adequate RNA concentration and A260/A280 ratio. The genome size of the fig wasp C. solmsi is typical of insects, but has undergone dramatic reductions of gene families involved in environmental sensing and detoxification. A conditional P value was calculated for each gene family, and families with conditional P values less than threshold (0.0001) were considered as having an accelerated rate of gain or loss. c. predation, where species 2 is the predator, species 1 the prey. To evaluate the assembly, we employed CEGMA and EST evaluations. Ramrez, S. R., et al. The authors declare that they have no competing interests. Most symbioses are obligate such as the symbiotic association of algae and fungi to form lichens. In this system, a large species (host) usually interacts with a smaller one (symbiont), which may live inside it as an endosymbiont. Ann Entomol Soc Am 96:716722, Pellmyr O, Thompson JN (1992) Multiple occurrences of mutualism in the yucca moth lineage. Suen G, Teiling C, Li L, Holt C, Abouheif E, Bornberg-Bauer E, Bouffard P, Caldera EJ, Cash E, Cavanaugh A, Denas O, Elhaik E, Fave MJ, Gadau JD, Graur D, Graur D, Grubbs KJ, Hagen DE, Harkins TT, Helmkampf M, Hu H, Johnson BR, Kim J, Marsh SE, Moeller JA, Munoz-Torres MC, Murphy MC, Naughton MC, Nigam S, Overson R, et al: The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. Most herbivorous insects have an antagonistic relationship with their host plants [2], but mutualistic fig wasps develop inside benign hosts. The genders exhibit extreme intraspecific morphological divergence in the compound eyes, wings, antennae, body color, and size, as expected given their functional adaptations to different life histories (Figure2). When the LRT was significant, a Bayes Empirical Bayes (BEB) analysis was conducted to identify putatively positively selected sites, which may also be relaxed selected sites though. Most insects have similar numbers of genes involved in detoxification [18], except for the honeybee, which has far fewer genes associated with xenobiotic metabolism. Thus, the Gr, Or, and OBP families in fig wasps appear to have experienced dramatic contractions relative to other insects. Four insect genomes including C. solmsi were compared. The rRNAs were found by aligning with blastn against a ref rRNA sequence from the closest related species. PLoS Biol 6:e59, CrossRef Proc R Soc B 272:25932599, Sakai S (2002) A review of brood-site pollination mutualism: plants providing breeding sites for their pollinators. Miyamoto T, Slone J, Song X, Amrein H: A fructose receptor functions as a nutrient sensor in the Drosophila brain. Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Patel RT, Soulages JL, Hariharasundaram B, Arrese EL: Activation of the lipid droplet controls the rate of lipolysis of triglycerides in the insect fat body. 1996. Non-mutualistic yucca moths and their evolutionary consequences. In addition, fig wasps must rapidly locate a chemically signaling host within their short free-living stage [14] (Figure1). Science. Thanks go to Prof. En-Kui Duan in Institute of Zoology, Chinese Academy of Sciences for helping in the analysis of the ommatidium structure of fig wasp. Phylogenetic analyses were conducted using maximum likelihood (ML) and Bayesian inference (BI). To annotate genes involved in the development of eyes and wings, proteins putatively participating in development of eyes and wings described for D. melanogaster were used as query sequences. To understand the gene composition of the chemosensory toolbox of fig wasps, we examine five gene families that mediate detection of chemical cues [28]: gustatory (Gr), olfactory (Or), and ionotropic receptors (Ir); odorant binding proteins (OBPs); and chemosensory proteins (CSPs) (Table2). Genomic DNA was sheared into fragments and seven libraries were constructed with inserted fragment sizes ranging from 200bp, 500bp, 800bp, 2kb, 5kb, and 10kb to 20kb by the manufacturers library kit (Illumina) [50]. 2008, 3: e3542-10.1371/journal.pone.0003542. The DNA was dissolved in 50L of TE buffer and stored at 80C. The contrast with other herbivorous insects is also striking. Proc Natl Acad Sci U S A 92:68646867, CrossRef Obligate Mutualism in an Extended Consumer-Resource Framework The transcriptome data reported in this paper were deposited in the National Center for Biotechnology Information Short Read Archive [95] under the accession no. PCR amplification of the sequences spanning the transferred fragment plus its flanking region confirms one candidate fragment in scaffold 108 that is similar to UDP-N-acetylmuramoylalanine-D-glutamate ligase of Wolbachia endosymbiont wVitB, although it cannot be translated due to a premature stop codon. The sex of larva individual was then confirmed by PCR of the male-specific splice isoform of doublesex. How to become a yucca moth: minimal trait evolution needed to establish the obligate pollination mutualism. This type of argument leads creationists into logical mires. Our annotation also includes 64 microRNAs, 138 tRNAs, 39 rRNAs, and 19 small nuclear RNAs in the genome of C. solmsi (Additional file 1: Table S6). Tijdschr Entomol 112:113, Gaunt MW, Miles MA (2002) An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographical landmarks. Obligate Pollination Mutualism pp 249270Cite as, Part of the Ecological Research Monographs book series (ECOLOGICAL). Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, Gerlach D, Kriventseva EV, Elsik CG, Graur D, Hill CA, Veenstra JA, Walenz B, Tubio JMC, Ribeiro JMC, Rozas J, Johnston JS, Reese JT, Popadic A, Tojo M, Raoult DL, Reed DL, Tomoyasu Y, Kraus E, Mittapalli O, Margam VM, et al: Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. https://doi.org/10.1007/978-4-431-56532-1_13, DOI: https://doi.org/10.1007/978-4-431-56532-1_13, eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0). 2010, 59: 307-321. Its very easy to adapt it to a Biblical chronology. 2000, 407: 81-86. PubMed Biol J Linn Soc 116:507518, Kephart S, Reynolds RJ, Rutter MT, Fenster CB, Dudash MR (2006) Pollination and seed predation by moths on Silene and allied Caryophyllaceae: evaluating a model system to study the evolution of mutualisms. 2013, 496: 57-63. (PDF) Landscape genomics of an obligate mutualism: discordant Google Scholar, Jandr KC, Herre EA, Simms EL (2012) Precision of host sanctions in the fig treefig wasp mutualism: consequences for uncooperative symbionts. The threshold was raised when protein sequences were short and few blast hits were found. d. lingering competition. Then 3L Proteinase K was added to the mixture, followed by 2h incubation at 58C. Unlike many other intimate symbioses, which involve vertical transmission of symbionts to host offspring, female fig wasps fly great distances to transfer horizontally between hosts. Dev Cell. Morphologically, the genders exhibit extreme differences in their compound eyes, wings, antennae, and body color. Google Scholar, Addicott JF, Bao T (1999) Limiting the costs of mutualism: multiple modes of interaction between yuccas and yucca moths. The fig wasp genome has a higher overall Ka/Ks ratio than other insects (mean omega values: C. solmsi, 0.039; Tribolium castaneum, 0.004; N. vitripennis, 0.026; A. mellifera, 0.028; Camponotus floridanus, 0.029; paired Wilcoxon rank sum tests: P <0.0001) (Additional file 1: Figure S3), indicating its faster proteins evolution. Mutualism | Types, Examples, & Facts | Britannica (A) Gene expression profiles with highly expressed genes shown in red, moderately expressed genes in black, and low or unexpressed genes in green. Show transcribed image text. Several evolutionary theorists have concluded that mutualism is more prevalent in the animal kingdom than previously assumed: "Mutualism may be the most prevalent form of cooperation; it occurs frequently across a wide variety of taxa" (Stevens et al. In many cases, ultimate response to partner removal cannot . For each adult group, we used 50 individuals. They also likely had certain pre-existing traits such as a preference for woody monocots in arid habitats, larval feeding in flower ovaries, and a specialized cutting ovipositor (Yoder, Smith, and Pellmyr 2010). Fazzari M, Greally J: Introduction to epigenomics and epigenome-wide analysis. To improve the integrity and correctness of the genome, transcriptome reads were aligned against the genome using TopHat to identify candidate exon regions and the donor and acceptor sites. 1994. So, as an example of an obligatory pollination relationship, Vanilla doesnt work well. PubMedGoogle Scholar. Honeybees have the smallest number of P450 genes (with 46) among previously characterized insect genomes. New Phytol 203:11091018, Song B, Stcklin J, Gao Y-Q, Peng D-L, Song M-S, Sun H (2016) Oviposition by mutualistic seed-consuming pollinators reduces fruit abortion in a recently discovered pollination mutualism. Thus, the absence of genes in these gene families was not due to incomplete annotation. So, Vanilla as a genus may have been pre-Flood (possibly a post-Creation, pre-Flood diversification) or it may have been a post-Flood development within the orchid kind. Fig-pollinating wasps (Agaonidae: Hymenoptera), hereafter referred to as fig wasps or fig pollinators for brevity, have an obligate, pollinating mutualism with fig trees (Ficus: Moracae) [12, 13]. Effects of gene flow on phenotype matching between two varieties of Joshua tree (. 2003, 19: 651-652. Its likely there are distinct species of such cheaters within the yucca moth genera (Pellmyr, Leebens-Mack, and Huth 1996). Genes that can trigger JAK/STAT (upd3) or JNK (eiger, wengen) signaling are absent in the chalcid genomes. A PCR-free library was also constructed. For RNA-seq, beads with oligo(dT) were used to isolate poly(A) mRNA. 1994. For CEGMA (version 2.4) [19] evaluation, we used 248 ultra-conserved core eukaryotic genes (CEGs) that were widely distributed and conserved in species to assess the completeness of genome assembly and gene-set. However, some gene fragments appear to have apparent bacterial or viral origins. BBA-General Subjects. Google Scholar. Symbionts that keep intimate contact with their hosts often show genome reduction, but it is not clear if the wide dispersal of female fig wasps will counteract this general tendency. Thus, we compare immune pathway models of the annotated draft genome with those of honeybees, jewel wasps, and four other insects (Additional file 1: Table S11). The story itself is flawed, as there is evidence that the bee species that pollinates the vanilla orchid in the wild is actually one of the larger euglossine bees (Ackerman 1983). Convergence of results was checked by Tracer[78] and two independent runs were performed to confirm convergence. Species Interactions and Competition | Learn Science at Scitable - Nature Gamma prior and alpha parameters were computed based on the substitution rate per time unit estimated by PAML baseml. Pellmyr, O., J. N. Thompson, J. M. Brown, and R. G. Harrison. Obligative mutualism | biology | Britannica Our manual annotation fails to discover significant divergences between the fig wasp and other insects in genes potentially involved in the development of compound eyes and wings (Additional file, section of development of compound eyes and wings). the predicted shape of the plant-mass lines if the species 2 plant was a parasite of the species 1 plant. Science. The fig acts as a nursery for developing fig wasp larvae, each of which consumes one presumptive seed (Figure1). 2000. Figure5 provides descriptions of the samples. 2000, 28: 45-48. These genes occur in three major functional classes: dietary/detoxification; hormone/semiochemical processing; and neuro-developmental/cell adhesion [39]. We sampled trees every 100 generations and discarded the initial 25% of the total trees as burn-in. This is obligate mutualism. About 1 month later, when the offspring were mature, we transferred several mated female daughter fig wasps into other bagged figs at their receptive stages. Yoder, J. Two independent approaches were used to identify possible HGT events. Aliso 24:97104, Lopez-Vaamonde C, Rasplus JY, Weiblen GD, Cook JM (2001) Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasites. Chronica Botanica Co., Waltham, Cornille A, Underhill JG, Cruaud A, Hossaert-McKey M, Johnson SD, Tolley KA, Kjellberg F, van Noort S, Proffit M (2012) Floral volatiles, pollinator sharing and diversification in the figwasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa). Li X, Schuler MA, Berenbaum MR: Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. From a creationist perspective, this suggests that the original expression of the yucca moths tentacular appendage could have arisen rapidly.. We used SOAPdenovo (version 2.01) to assemble the genome with the following procedures (basic information in Table1; details are referred to the giant panda [50]): construct contig: split the short-insert size library data into 43-mers and construct a de Bruijn graph. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Gotzek D, Robertson HM, Wurm Y, Shoemaker D: Odorant binding proteins of the red imported fire ant. Within yucca mothyucca plant mutualism, for example, the yucca moth provides a service (pollination) while the yucca plant provides a resource (seeds in which the yucca moths eggs grow). Data for this Whole Genome Shotgun project were deposited at DDBJ/EMBL/GenBank under the accession no. More than two-thirds of pollinating yucca moth species are associated with only a single species of. JHW, DW, LMN, GCM, TT, SNB, NXW, CYY, NW, YGF, SVY, XYY, QZ, CXL, CYX, LJH, LLY, MC, YZ, SWW, SZ, YHL, YYY, XJQ, YC, LLB, SZ, JYW, YY, HX, GHW, HY, WSW, and JW analyzed the data. Herre EA, Knowlton N, Mueller UG, Rehner SA: The evolution of mutualisms: exploring the paths between conflict and cooperation. CAS Cite this article. Nature 376:557558, Riley CV (1872) The fertilization of the yucca plant by Pronuba yuccasella. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Both genes are intact without introns. Researchers discovered that European honeybees were effectively pollinating the flowers. 2005, 280: 22624-22631. 10.1038/nature06784. DNA extraction occurred immediately on arrival.
